Different effects of warming and cooling on the ... · 2011). Because the soil carbon (C) pool is...

Different effects of warming and coolingon the decomposition of soil organic matter in warm–temperate oak forests: a reciprocal translocation experiment

Junwei Luan • Shirong Liu • Scott X. Chang •

Jingxin Wang • Xueling Zhu • Kuan Liu •

Jianghua Wu

Received: 16 September 2013 / Accepted: 1 August 2014 / Published online: 5 September 2014

� The Author(s) 2014. This article is published with open access at Springerlink.com

Abstract A reciprocal soil monolith-transfer exper-

iment was conducted along an altitude gradient to

investigate the effect of climate change on soil carbon

(C) processes in two warm–temperate oak forests in

Baotianman Nature Reserve, Henan Province, China.

Microclimate conditions, soil surface CO2 flux, and

labile organic C were measured for in-situ and

transferred soils at both high and low-elevation sites.

The soil temperature at 5 cm depth was, on average,

3.27 �C warmer at the low-elevation site than at the

high-elevation site. Net CO2 flux (911 g C m-2

13 months-1, 4.7 % of total C) of soil monoliths

transferred from the high to the low-elevation site

(simulating warming) was substantially (44 %)

greater than for high-elevation soil monoliths incu-

bated in situ (633 g C m-2 13 months-1, 3.3 % of

total C) during 13 months of incubation. Increased

extractable organic C (K2SO4-C) supply with warm-

ing partly explained the increase of soil CO2 flux.

Simulated warming also significantly increased the

temperature sensitivity (Q10 values) of soil organic

matter decomposition. The positive linear relationship

between microbial metabolic quotient (qCO2) and Q10

suggests a connection between microbial populationResponsible Editor: Kathleen Lohse.

J. Luan � S. Liu (&)

The Research Institute of Forest Ecology, Environment

and Protection, Chinese Academy of Forestry, Key

Laboratory of Forest Ecology and Environment, China’s

State Forestry Administration, Beijing 100091, People’s

Republic of China

e-mail: [email protected]

J. Luan


J. Luan � J. Wu

Sustainable Resource management, Grenfell Campus,

Memorial University of Newfoundland, Corner Brook,

NL A2H 6P9, Canada


S. X. Chang

Department of Renewable Resources, University of

Alberta, Edmonton, AB T6G 2E3, Canada


J. Wang

Division of Forestry and Natural Resources, West

Virginia University, Morgantown, WV 26506, USA


X. Zhu

Baotianman Natural Reserve Administration,

Neixiang 474350, Henan, People’s Republic of China


K. Liu

Institute for Clinical Evaluative Sciences, ELL-108, 800

Commissioners Road, London, ON N6A 5W9, Canada


123

Biogeochemistry (2014) 121:551–564

DOI 10.1007/s10533-014-0022-y

and Q10 under warming conditions. Transfer of soil

monoliths from the low to the high-elevation site

(simulating cooling) substantially (30 %) reduced soil

CO2 flux (383 g C m-2 13 months-1, 2.5 % of total

C) compared with those incubated in situ

(550 g C m-2 13 months-1, 3.5 % of total C). How-

ever, this was not accompanied by consistently

opposite changes, to a similar extent, in labile organic

C (microbial biomass carbon and K2SO4-C) and

decomposition results (i.e., Q10 and R10, soil respira-

tion at 10 �C), indicating that the soil organic matter

decomposition process may not respond equally to

cooling and warming. Different soil organic matter

decomposition responses to cooling and warming

should be considered for paleoecological modeling

when both warming and cooling are involved in the

changes in regional and global climates, particularly

during the Holocene.

Keywords Climate warming � Simulated cooling �CO2 flux � Q10 � Soil organic carbon decomposition �Microbial metabolic quotient

Introduction

The decomposition of organic matter (OM) is a

fundamental global biogeochemical process, because

it is important in the recycling of nutrients between

soil and plant communities. Changes in the rates of

OM decomposition can have profound effects on

ecosystem function and productivity (Salinas et al.

2011). Because the soil carbon (C) pool is much larger

than the atmospheric C pool, even a small change in

the rate of decomposition of the large soil organic C

pool could have a significant effect on atmospheric

CO2 concentrations (Bottner et al. 2000). However,

soil OM decomposition (Davidson and Janssens 2006)

and microbial population size and functional group

composition (Zhang et al. 2005; Zogg et al. 1997) are

strongly temperature dependent. Therefore, an

increase in the global mean annual temperature of

1.5–4.5 �C over the next 50–100 years is likely to

have a substantial effect on the terrestrial ecosystem C

cycle (IPCC 2007). Understanding the response of soil

OM decomposition to climate change is a critical

aspect of ecosystem responses to global changes

(Conant et al. 2011).

A large number of warming experiments have been

conducted to elucidate the effects of global warming

on soil OM decomposition (Hopkins et al. 2012; Knorr

et al. 2005; Luo et al. 2001; Melillo et al. 2002).

However, the possibility of a cooler and wetter future

climate is rarely considered in global climate change

research, although rapid cooling events have occurred

during the Holocene (Mayle and Cwynar 1995) and

seasonal cooling is also frequently a part of the inter-

annual variability of the climate (Brando et al. 2010;

Le Barbe et al. 2002; Liang et al. 2011). It is still not

clear whether or not this opposite process (i.e.,

cooling) will have an effect on soil OM decomposition

opposite to that of warming.

Several field experimental approaches have been

used to investigate potential effects of global warming

on the ecosystem, for example field warming using

external heat inputs (Luo et al. 2001; Melillo et al.

2002), observing differences in ecosystems along

natural climatic gradients (Conant et al. 2000; Rodeg-

hiero and Cescatti 2005), or transferring ecosystem

components to a new site with different climatic

conditions (Breeuwer et al. 2010; Hart 2006; Link

et al. 2003; Rey et al. 2007). Especially, reciprocal

treatment (simulating climate cooling) to that of

warming can strengthen the conclusions drawn from

warming treatment in which temperature has a dom-

inant effect on soil–plant processes (Hart and Perry

1999). Reciprocal soil translocation experiments have

been widely used to understand the potential effects of

climate change on C and nitrogen (N) cycles (Hart

2006; Hart and Perry 1999; Link et al. 2003; Rey et al.

2007; Zimmermann et al. 2009) and soil microbial

communities (Budge et al. 2011).

The Baotianman Nature Reserve in Henan Prov-

ince, China, is located in the transitional region

between the northern subtropics and the warm-

temperate zone. Previous research in this region

revealed that the seasonality of soil temperature was

the main condition affecting seasonal variation of soil

CO2 flux (Luan et al. 2011a); its effect was even larger

than that of soil moisture availability (Luan et al.

2012). This is a region in which the effects of climate

change are expected to be substantial but the effect of

warming on soil OM decomposition is poorly under-

stood. The reserve has elevation range in excess of

1,400 meters with a 3–5 �C difference in soil temper-

ature between low and high-elevation sites. We used

the altitude gradient along the slopes of the

552 Biogeochemistry (2014) 121:551–564

123

Baotianman Nature Reserve to conduct a reciprocal

soil monolith translocation experiment to simulate

temperature changes (i.e., warming and cooling). We

hypothesized that both warming and cooling (with the

same extent of temperature change) will affect soil

CO2 flux, labile organic C, and decomposition behav-

ior, and that changes in labile organic C could explain

the effect of soil CO2 flux caused by simulated climate

change. Our specific objectives were to: (1) investigate

the response of soil CO2 flux to reciprocal soil

monolith transfer treatments; and (2) assess how labile

organic C and decomposition parameters (i.e., soil

respiration at 10 �C, R10; temperature sensitivity of

soil OM decomposition, Q10; microbial metabolic

quotient, qCO2) respond to simulated cooling as

compared with simulated warming treatments.

Materials and methods

Study sites

Two sites (a high-elevation site and a low-elevation site)

located in the Baotianman Natural Reserve in

Henan Province, China, were selected to conduct the

reciprocal transfer experiment. The high-elevation site

(33�2905100N, 111�5505800E) was located approximately

1,400 m.a.s.l., with a slope\8 %. The site was occupied

by secondary forest regenerated from a clear-cut harvest

approximately 50 years ago, with Quercus aliena var.

acuteserrata as the dominant species. In addition to the

dominant species, other abundant tree species include

Carpinus cordata, Cornus controversa Hemsl, and Tilia

americana. Annual average precipitation and air tem-

perature measured at a nearby weather station were

900 mm and 15.1 �C, respectively. Precipitation mainly

falls from June to August. Soils were dominated by a

Ferric Luvisols, on the basis of the FAO system of soil

classification (FAO 1990). The low-elevation site

(33�2805500N, 111�52052.800E) was located at approxi-

mately 620 m.a.s.l., with a slope\10 %. The forest at

this site was regenerated from a clear-cut harvest

approximately 30 years ago. The dominant species at

this site was Quercus variabilis B. Other abundant tree

species include C. controversa Hemsl., Toxicodendron

vernicifluum (Stokes) F. A. Barkl., and Quercus serrata

var. brevipetiolata (A. DC.) Nakai. Annual average

precipitation and air temperature were ca. 800 mm and

19.8 �C, respectively. Precipitation mainly occurs from

June to August. Soils were dominated by a Chromic

Luvisol, on the basis of the FAO system of soil

classification (FAO 1990). The basic stand attributes

of the two sites are summarized in Table 1.

Experimental design

In July 2008, eight 3 9 3 m plots were established

randomly at both the high and low-elevation sites.

Three intact soil monoliths (30 cm diameter, 40 cm

deep from the surface of the O horizon) were collected

from adjacent locations within each plot, with the least

possible disturbance, by use of PVC cylinders. The

first monolith collected was returned to the laboratory

for processing, the second monolith was returned to its

original location within the site (in-situ soil monolith,

ISHE: high-elevation soil monoliths incubated in situ;

ISLE: low-elevation soil monoliths incubated in situ),

and the third monolith was transferred to the other

forest site for incubation (transferred soil monolith,

TRH-L: a soil monolith transferred from the high to the

low-elevation site; TRL-H: a soil monolith transferred

from the low to the high-elevation site). At each site,

four 1 9 1 m plots trenched to 0.6 m depth on the

perimeter were established to check on the soil coring

effect (trenched). One PVC collar (19.6 cm in diam-

eter) was installed permanently in each soil monolith

(centric avoiding edge effect) or trenched plot.

Because one of the soil monoliths to be transferred

from the low to the high-elevation site was lost during

the translocation process, this experimental design had

eight replicates for the high-elevation site and seven

replicates for the low-elevation site, per treatment

(incubated in situ or transferred) and four replicates for

the trenching treatment. Vegetation (grasses and

saplings) which occasionally grew in the monolith at

the beginning of and during the experiment was

manually removed. The soil water content of the

monoliths incubated in the high-elevation site was

much higher than that of those incubated in the low-

elevation site. Therefore, we conducted a precipitation

exclusion experiment at the high-elevation site for

both the ISHE (n = 4) and TRL-H (n = 3) treatments to

further investigate the effect of soil water content on

soil CO2 emission, starting from August 15, 2009.

Translucent roofs, each 3 9 3 m, were constructed

and placed 1.6 m above the soil monoliths to exclude

the rainfall.

Biogeochemistry (2014) 121:551–564 553

123

Soil respiration, temperature, and moisture content

Soil respiration was measured from September 2008 to

November 2009, by use of an Li-8100 soil CO2 flux

system (Li-Cor, Lincoln, NE, USA) for each soil

monolith. Soil temperature at 5 cm depth from the soil

surface (T5) was measured adjacent to each respiration

collar with a portable temperature probe provided with

the Li-8100. Soil volumetric water content at 0–5 cm

depth (SWC) was measured by use of an MPKit-B

portable time domain reflectometer soil moisture

meter (NTZT, Nantong, China) at three points close

to each collar. Measurements were made twice a

month, but no measurements were made in December

2008 and January and February 2009 because the

ground was covered with snow.

Soil and forest stand characteristics

Soil bulk density, organic C, total N, and pH were

determined for the initial samples collected in July

2008 (n = 8). Soil bulk density every 20 cm for the

40-cm-long monoliths was determined by use of

100 mL (50.46 mm diameter, 50 mm high, n = 3)

sampling corers and placing intact samples in an oven

at 105 �C for 24 h to determine soil water content.

Organic C content was determined by the wet

oxidation method with 133 mmol L-1 K2Cr2O7 and

digestion at 170–180 �C. Soil N concentration was

determined by a micro-Kjeldahl method (DK-152

Kjeltec Auto Analyzer; VELP, Italy) (Lu 2000).

At the end of the study period (August 29, 2010),

soil samples were collected from the 0–15 cm layer of

all monoliths, by use of a 2.54 cm diameter corer, to

determine soil microbial biomass C (MBC) and

K2SO4-extractable C (K2SO4-C) after 13 months of

treatment. Three cores were taken from each monolith

and mixed to form a composite sample. The samples

were kept in a cooler and delivered immediately to the

laboratory for analysis. The samples were kept at 4 �C

in a refrigerator before determination of MBC by use

of the chloroform fumigation–extraction method;

MBC was calculated by dividing the fumigation

C-flush by a KEC factor of 0.45 (Sparling et al.

1990). Each sample was extracted with 0.5 mol L-1

potassium sulfate (K2SO4) to determine K2SO4-C, as

described by Weintraub et al. (2007).

Tree diameter at breast height (DBH) was measured

1.3 m from the ground for each tree in both sites. LeafTa

ble

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123

area index (LAI) was measured in August 2009 along

a 25 m transect in each stand, by use of WinSCAN-

OPY (Regent Instruments, Quebec, Canada).

Data analysis

Numerous equations have been developed to express

the temperature sensitivity of respiration (Kirschbaum

2000; Janssens and Pilegaard 2003). We first used the

most common expression (Davidson et al. 2006), the

van’t Hoff equation (Eq. 1), to describe the relation-

ship between soil respiration (RS) and soil temperature

at 5 cm depth (T5):

RS ¼ aebT5 ; ð1Þ

where RS is soil respiration rate, T5 is the soil

temperature at 5 cm depth, a and b are fitted variables,

and R10 is defined as the respiration rate at 10 �C. The

temperature-sensitivity variable, Q10, was calculated

by use of the equation:

Q10 ¼ e10b: ð2Þ

We then used the Lloyd and Taylor (1994) function:

RS ¼ a� e�E0= T5�T0ð Þ; ð3Þ

where a, E0, and T0 are fitted variables, and T5 is the

soil temperature at 5 cm depth.

It has been suggested that this function is a better

and unbiased expression of the relationship between

respiration and soil temperature than the standard

Arrhenius function (Fang and Moncrieff 2001) for

fitting measured soil respiration rates and soil temper-

ature data. Temperature sensitivity, as expressed by

Q10 values, was then calculated by comparing respi-

ration rates at 5 �C above and below the site specific

mean annual temperature (T5), as described in Zim-

mermann et al. (2010):

Q10 ¼ RT5þ5

�RT5�5

: ð4Þ

Soil microbial respiration (the total soil respiration

reported in this study, because vegetation was

excluded so there was no autotrophic respiration in

our monoliths) and soil microbial biomass was used to

calculate the microbial metabolic quotient (qCO2),

which is the amount of CO2–C produced per unit of

microbial biomass carbon (Anderson and Domsch

1993; Wardle and Ghani 1995).

Comparisons of soil monoliths collected from the

high-elevation site and incubated in situ with those

transferred and incubated at the low-elevation site

were made to assess the potential effects of global

warming on soil pools and processes. The soil

monoliths collected from the low-elevation site and

incubated in situ was compared with those transferred

to the high-elevation site to evaluate the simulated

cooling effect on these pools and processes. Compar-

ison of measurements made on soil monoliths incu-

bated in situ with those made on ambient trenched soil

was used to test the potential effect of soil contain-

ment on soil microclimate and on CO2 flux at each

site.

A repeated-measures general linear model (GLM)

was used to evaluate the effects of the treatments

(ambient trenched, in situ, and transferred) on RS,

SWC, and T5. One-way analysis of variance

(ANOVA) was used to evaluate the effects of the

treatments (in situ, transferred) on MBC and K2SO4-C

measured at the end of the study period, and R10, Q10,

and qCO2 values. General linear models were used to

assess the effect of soil origin, incubation site, and

their interaction effects. Linear regression analysis

was performed between CO2 flux (average between

August 13 and September 17, 2009, which were the

days closest to the soil sampling day for K2SO4-C and

MBC analysis) and K2SO4-C and MBC, and between

Q10 values and qCO2. All statistical analysis was

performed by use of SPSS 13.0 software for Windows

(SPSS, Chicago, USA).

Results

Soil micro-environment

T5, measured at the same time as CO2 flux, was higher

(a warming effect) for TRH-L (mean = 16.54 �C) than

for ISHE (13.27 �C) (P \ 0.01, Fig. 1a) and lower (a

cooling effect) for TRL-H (13.31 �C) than for ISLE

(16.99 �C) (P \ 0.01, Fig. 1b). SWC was lower for

TRH-L (0.23 cm3 cm-3) than for ISHE (0.27 cm3 -

cm-3) (P \ 0.01, Fig. 1c) but higher for TRL-H

(0.27 cm3 cm-3) than for ISLE (0.24 cm3 cm-3)

(P \ 0.01, Fig. 1d), indicating wetter conditions in

the high-elevation site than in the low-elevation site.

T5 for trenched and in-situ treatments for both sites

was no different (Fig. 1a, b), and we did not find


123

significant differences between SWC for in-situ and

trenched treatments at the low-elevation site (Fig. 1d).

No clear seasonal trend was observed for T5 or SWC

differences between the transferred and in-situ treat-

ments for monoliths from high and low-elevation sites

(Fig. 1a–d).

CO2 flux

Transfer of soil monoliths from the high to the low-

elevation site resulted in an increase in CO2 flux of

approximately 44 % over the 13-month incubation

period compared with ISHE (911 and 633 g C m-2

a

2008

250 300 350

T5

(o C)

-10

-5

0

5

10

15

20

25transferred A

in situ B

trenched B

transferred-insitu

High-elevation soil

2009

50 100 150 200 250 300

b

2008

250 300 350-10

-5

0

5

10

15

20

25

c

2008

250 300 350

Soi

l wat

er c

onte

nt (

cm3 c

m-3

)

-0.2

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

2009

50 100 150 200 250 300

ABCtransferred-insitu

d

2008

250 300 350-0.2

-0.1

0.0

0.1

0.2

0.3

0.4

0.5

2009

50 100 150 200 250 300

ABABtransferred-insitu

e

2008

250 300 350

RS (

µ m

ol C

O2

m-2

s-1)

-2

-1

0

1

2

3

4

5

6

7

2009

50 100 150 200 250 300

ABBtransferred-in situ

f

2008

250 300 350-2

-1

0

1

2

3

4

5

6

7

2009

50 100 150 200 250 300

ABCtransferred-in situ

DOY DOY

Low-elevation soil

2009

50 100 150 200 250 300

transferred A

in situ B

trenched B

transferred-insitu

Fig. 1 Seasonal patterns of soil temperature at 5 cm depth (T5)

and soil water content (SWC) among different treatments for the

high and low-elevation sites. Soils were subjected to three

treatments: transferred (soil monoliths incubated at the other

forest site), in-situ (soil monoliths incubated in situ), and

trenched (trenched to exclude root growth). The difference

between transferred and in situ measurements is plotted as bars.

For a given soil sample, treatments followed by different

superscript letters denote significant differences (P \ 0.05)

among treatments (RM ANOVA, Tukey’s test). Vertical bars

denote SE of the mean (n = 8 or 7 for high or low-elevation sites,

respectively). Net CO2 flux from soils for e high and f low-

elevation oak forest sites. Vertical bars denote SE of the mean

(n = 8 or 7 for high or low-elevation sites, respectively)


123

13 months-1, respectively). Transfer of soil mono-

liths from the low to the high-elevation site, however,

resulted in a decrease in net CO2 flux of approxi-

mately 30 % compared with ISLE (383 and

550 g C m-2 13 months-1, respectively). Soil con-

tainment had no effect on net CO2 flux from soil

monoliths at the high-elevation site, whereas a

reduction was found at the low-elevation site (Fig. 1e,

f). The difference between soil CO2 flux for the

transferred and in-situ treatments for both the high and

low-elevation sites had similar seasonal patterns to

those of soil temperature (Fig. 1e, f). T5 is a good

indicator for explaining the seasonal variation of CO2

flux in the transferred and in-situ treatments for both

the high and low-elevation sites (R2 = 0.84–0.89,

P \ 0.001; Fig. 2a, b), whereas SWC had no rela-

tionship with seasonal variations of CO2 flux for each

treatment (Fig. 2c, d). Exclusion of precipitation led

to a rapid decrease of SWC and soil CO2 flux, which

were significantly different between the control and

the precipitation exclusion treatments (Fig. 3).

Results for soil decomposition and labile organic C

Transfer of soil monoliths from the high to the low-

elevation site reduced soil MBC and increased Q10

values (calculated on the basis of both the van’t Hoff

and Lloyd and Taylor equations), K2SO4-C, and qCO2

compared with the ISHE treatment (P \ 0.05,

Table 2). In contrast, transferring soil monoliths from

the low to the high-elevation site did not affect Q10,

K2SO4-C, and MBC (Table 2). Soil origin signifi-

cantly affected K2SO4-C, MBC, and R10, but not Q10

values (calculated on the basis of both the van’t Hoff

and Lloyd and Taylor equations) and qCO2 (Table 3).

In contrast, incubation site significantly affected Q10,

MBC, and qCO2 (Table 3). Significant linear relation-

ships were found between qCO2 and Q10 values

calculated by use of both the van’t Hoff and Lloyd and

Taylor equations (Fig. 4).

Discussion

Soil micro-environment

In our study, significant exponential relationships

between soil respiration and soil temperature (Fig. 2a,

b) and lack of relationships between soil respiration

and soil moisture content (Fig. 2c, d) illustrate that soil

temperature was the dominant factor regulating soil

organic matter decomposition in the forest ecosystems

a

T5 (oC)

0 5 10 15 20 25R

µS (

mol

CO

2 m

-2s-1

)0

1

2

3

4

5

6

7

transferred (TRH-L)

y = 0.293e0.123x

R2 = 0.88, P < 0.001in situ (ISHE)

y = 0.407e0.102x

R2 = 0.89, P < 0.001

b

T5 (oC)

0 5 10 15 20 250

1

2

3

4

5

6

7

transferred (TRL-H)

y = 0.256e0.096x

R2 = 0.84, P < 0.001in situ (ISLE)

y = 0.196e0.116x

R2 = 0.86, P < 0.001

High-elevation soil Low-elevation soil

c

Soil water content (cm3 cm-3)

0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40

Rµ

S (

mol

CO

2 m

-2s-1

)

0

1

2

3

4

5

6

7

d

Soil water content (cm3 cm-3)

0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.400

1

2

3

4

5

6

7

High-elevation soilLow-elevation soil

Fig. 2 Relationships

between soil CO2 flux and

soil temperature at 5 cm

depth for soil monoliths

originally from a the high-

elevation site and b the

low-elevation site.

Relationships between soil

CO2 flux and soil water

content for soil monoliths

originally from c the high-

elevation site and d the

low-elevation site


123

studied, similar to previous studies of those ecosys-

tems (Luan et al. 2011a, b). Therefore, the appreciable

response of soil respiration to the translocation

treatment (Table 2) was mainly caused by changes

in soil temperature rather than soil moisture content,

even though there was a significant treatment effect on

soil moisture content (Fig. 1c, d). In this study, SWC

ranged between 0.15 and 0.35 cm3 cm-3 (except on

July 4th when it dropped below 0.10 cm3 cm-3),

which was likely to be within the optimum range for

soil microbial activity (Luan et al. 2012). In our

precipitation exclusion experiment, CO2 flux

decreased after the SWC dropped to a critically low

value (e.g., 0.15 cm3 cm-3; Fig. 3). These results

further illustrate that soil temperature change had a

crucial effect on responses of soil organic matter

decomposition to the transfer treatment. In addition,

the lack of containment effects on soil temperature in

either the high or low-elevation sites indicates that we

can exclude the containment effect on soil respiration

from our analysis, enabling us to conduct the follow-

ing more detailed analyses.

Soil CO2 flux

Our hypothesis that both warming and cooling affect

soil CO2 flux is supported by the results of this study

(Table 2). Soils in the high-elevation site will be

vulnerable to large C losses under future warming

conditions. Simulated warming led to 44 % more C

being released as CO2 whereas simulated cooling led

to 30 % less C being released as CO2 during the

13 months incubation, indicative of different effects

of cooling and warming of the soils studied. Different

soil characteristics between the high and low-eleva-

tion sites (Table 1) might have led to the different

responses. Higher qCO2 in the warmer site (Table 2)

might also explain the increase of CO2 flux, as a

positive linear relationship was found between qCO2

and CO2 flux, irrespective of soil origin and incubation

b

2009

50 100 150 200 250 300

d

2009

50 100 150 200 250 300

c

2009

50 100 150 200 250 300

a

2009

50 100 150 200 250 300

Low-elevation soil, Transferred

2008

250 300 350

Soi

l wat

er c

onte

nt (

cm3 c

m-3

)

0.1

0.2

0.3

0.4

High-elevation soil, in situ

2008

250 300 350

Rµ

S (

mol

CO

2 m

-2s-1

)

0

1

2

3

4

Low-elevation soil, Transferred

2008

250 300 350

Rµ

S (

mol

CO

2 m

-2s-1

)

0

1

2

3

4

High-elevation soil, in situ

2008

250 300 350

Soi

l wat

er c

onte

nt (

cm3 c

m-3

)

0.1

0.2

0.3

0.4

ControlPrecipitation excluded

*

***

*

**

****

**

*

**

DOY DOY

* **

*** *

Aug. 15 Aug. 15

Aug. 15 Aug. 15

Fig. 3 Seasonal pattern of soil water content (a) and soil

respiration (b) in control and precipitation exclusion treatments

for high-elevation soil monoliths incubated in situ (bars denote

SE of the mean, n = 4). Seasonal pattern of soil water content

(c) and soil respiration (d) in control and precipitation exclusion

treatments for low-elevation soil monoliths incubated at the high-

elevation site (bars denote SE of the mean, n = 3). * and **

denote significantly different SWC or RS between the control and

precipitation exclusion treatments at P \ 0.05 and P \ 0.01,

respectively


123

site (CO2 flux = 399.6 ? 14081 9 qCO2, R2 = 0.33,

P = 0.001).

Interestingly, CO2 flux rates were similar for the

two soils in their initial elevations even though there

were apparent differences in soil characteristics (i.e.,

lower SOC, K2SO4-C and MBC at the low-elevation

site, Table 2). In addition, if we do not consider the

direction of soil monolith transfer, both high and low-

elevation soils had 44 % greater CO2 flux when they

were incubated in the low-elevation site than those

incubated in the high-elevation site, indicating that the

temperature difference between the two sites deter-

mined the different CO2 flux rates. In combination

with higher soil C stock at the higher-elevation site

(Table 1), similar CO2 flux rate between both soils

incubated in situ implies that more C would be stored

in the soil at the high-elevation site (Zimmermann

et al. 2009, 2010).

Soil heterotrophic respiration is determined by

temperature and many other factors other than

temperature, for example C substrate supply, micro-

bial biomass, and climatic conditions (Davidson et al.

2006). In our study, a 3.27 �C soil temperature

increase led to a 44 % increase in soil CO2 flux,

which was much less than the 120 % increase reported

in a spruce–fir forest as the result of a 2.5 �C increase

in soil temperature (Hart 2006). The different

responses might be caused by different soil quality.

For example, the soil in the Hart (2006) study had a

higher C:N ratio (24.4–41) than that in our study

(14.6–15.6). Increased substrate availability was also

linked to the increase of CO2 flux caused by warming

in our study (Fig. 5a).

The transferred soils underwent a change in air and

soil temperatures, and soil CO2 flux rates. However, in

our reciprocal soil-transfer experiment, the transfer of

soil monoliths to either a warmer or cooler site resulted

in comparably stable seasonal warming or cooling

effects (soil temperature difference between trans-

ferred and in-situ treatments; Fig. 1a, b) and it was not

accompanied by similar stable seasonal variation of

differences in soil CO2 flux between the transferred

and in-situ treatments (Fig. 1e, f). Both warming and

cooling effects on soil CO2 flux were more apparent

during the summer, which could be attributed to

higher microbial activity in the summer when soil

moisture availability was not limiting (Martin and

Bolstad 2005). The effect was clearly demonstrated at

the high-elevation site (Table 2) where more substrate

supply occurred and substrate availability (e.g.,

Table 2 Reciprocal soil monolith transfer effects on soil

respiration rates at 10 �C (R10), Q10, K2SO4 extractable C,

microbial biomass C (MBC), and microbial metabolic quotient

(qCO2) of the high and low-elevation sites in Baotianman

National Nature Reserve

Soil treatment CO2 g C m-2

13 months-1R10 lmol CO2 m-2 s-1

van’t

Hoff

Q10

Lloyd and

Taylor Q10

K2SO4 C

mg g-1 soil

MBC

mg g-1

soil

qCO2 lg CO2 h-1 lg

microbial C-1

High-elevation soil

In situ

(ISHE)

633a (34) 1.12a (0.05) 2.73a

(0.46)

2.72a (0.19) 0.23a (0.03) 1.14a

(0.48)

0.010a (0.002)

Transferred

(TRH-L)

911b (85) 0.97a (0.07) 3.42b

(0.48)

3.75b (0.33) 0.27b (0.03) 0.73b

(0.08)

0.023b (0.003)

F 9.107 2.976 8.74 6.08 10.332 5.472 12.14

P value 0.009 0.107 0.01 0.007 0.006 0.035 0.004

Low-elevation soil

In situ

(ISLE)

550a (23) 0.61a (0.03) 3.10a

(0.28)

3.31a (0.11) 0.09a (0.04) 0.40a

(0.21)

0.019a (0.003)

Transferred

(TRL-H)

383b (23) 0.54a (0.06) 2.69a

(0.65)

3.03a (0.42) 0.10a (0.04) 0.59a

(0.19)

0.0065b (0.0006)

F 22.43 1.215 2.278 0.429 0.109 3.348 16.32

P value \0.001 0.292 0.157 0.525 0.746 0.092 0.002

ISHE, high-elevation soil monoliths incubated in situ; ISLE, low-elevation soil monoliths incubated in situ; TRH-L, high-elevation soil

monoliths transferred to the low-elevation site; TRL-H, low-elevation soil monoliths transferred to the high-elevation site

Values in parentheses are SE. Different lowercase letters within each column indicate significant difference at P = 0.05 level


123

K2SO4-C) has a strong effect on soil respiration

(Curiel Yuste et al. 2007; Grogan and Jonasson 2005).

Labile organic carbon

The significant reduction in MBC in the soil caused by

the warming treatment (Table 2) was consistent with

the effect of 12 years of soil warming of approxi-

mately 5 �C at the Harvard Forest (Bradford et al.

2008; Smith et al. 2004). However, the reduction in

microbial biomass did not imply a reduction in

substrate supply as there was a significant increase

in K2SO4-C, or a reduction in microbial activity as

CO2 flux increased after transfer from the high to

the low-elevation site (Fig. 5a). Our results partially

support the idea that the reduction in the increment

of respiration rates after prolonged soil warming

was caused by substrate loss (Kirschbaum 2004;

Knorr et al. 2005), because the increase of CO2 flux

eventually reduced substrate availability. Rey et al.

(2007) found that relative emissions per unit of C

depended mostly on climate and there was a clear

reduction of absolute emissions with decreasing

labile C content. The changes in CO2 flux after

translocation may also be attributed to the changes

in microbial metabolic quotient (Table 2) and shifts

in microbial community composition (Budge et al.

2011).

In contrast, transferring soil monoliths from the low

to the high-elevation site (i.e., cooling) did not result in

expected changes in MBC and K2SO4-C. It isTa

ble

3S

ign

ifica

nce

of

gen

eral

lin

ear

mo

del

(tw

o-f

acto

rA

NO

VA

)fo

rev

alu

atio

no

fso

ilo

rig

in(i

.e.,

hig

h-e

lev

atio

nv

s.lo

w-e

lev

atio

n),

incu

bat

ion

site

(i.e

.h

igh

-ele

vat

ion

vs.

low

-ele

vat

ion

)ef

fect

s,an

dth

eir

inte

ract

ion

sw

ith

soil

dec

om

po

siti

on

con

dit

ion

s(d

f=

1fo

ral

lfa

cto

rs)

Fac

tor

CO

2K

2S

O4

extr

acta

ble

CM

BC

R10

Van

’tH

off

Q10

Llo

yd

and

Tay

lor

Q10

qC

O2

Pv

alu

eF

Pv

alu

eF

Pv

alu

eF

Pv

alu

eF

Pv

alu

eF

Pv

alu

eF

Pv

alu

eF

So

ilo

rig

inef

fect

0.0

11

7.6

\0

.00

11

7.1

70

.07

3.5

90

.00

31

0.6

60

.47

0.5

50

.95

0.0

05

0.6

46

0.2

16

Incu

bat

ion

site

\0

.00

11

7.6

0.1

91

.82

0.0

17

.81

0.5

04

0.4

59

0.0

05

9.2

70

.03

45

.03

0.0

01

14

.79

So

ilo

rig

in9

Incu

bat

ion

site

0.3

04

1.1

0.0

72

3.5

0.3

21

.04

0.0

65

3.7

40

.43

0.6

44

0.2

11

.64

0.9

76

0.0

01

Cw

asin

clu

ded

inth

eG

LM

asa

cov

aria

tev

aria

ble

qCO2

0.00 0.01 0.02 0.03 0.04

Q10

1

2

3

4

5

6

7

8

Lloyd and Taylor Q10

y = 43.05x + 2.56, R2 = 0.23, P = 0.007van't Hoff Q10

y = 28.68x + 2.56, R2 = 0.24, P = 0.007

Fig. 4 Relationships between average CO2 flux (samples were

collected on Aug. 13 and Sept. 17 near fresh soil sampling day)

and K2SO4-C (a), and MBC (b) for soil monoliths originally

from the high and low-elevation sites


123

plausible that soils from the low-elevation site with

poor labile-C and a smaller microbial population, were

less responsive to the change in temperature, and

required a longer time to adapt to the new (cooler)

environment. We found that neither MBC nor K2SO4-

C could explain the reduction of CO2 flux after

transferring soil monoliths from the low to the high-

elevation site (Fig. 5a, b). Therefore, only part of our

hypothesis was supported—that warming will affect

labile organic C and subsequently CO2 flux; however,

the corresponding responses did not occur in the

cooling treatment, rejecting part of the hypothesis.

Temperature sensitivity of soil respiration

Q10 values increased when soil monoliths were

transferred from the high to the low-elevation site

(Table 2) and were affected by incubation site but not

by soil origin (Table 3), indicating a higher risk of C

loss under future warming conditions. We found a

significant linear relationship between Q10 values and

qCO2 (Fig. 4), suggesting a connection between

temperature sensitivity of soil organic matter decom-

position and soil microbial function under warming,

because qCO2 is a useful measure of microbial

efficiency in conserving C (Wardle and Ghani 1995).

Soil microbes that were adapted to the higher elevation

(lower temperature) reduced their biomass and

increased qCO2 when the soil was transferred to the

lower-elevation (higher-temperature) site. A moderate

shift of microbial communities toward new environ-

mental conditions 11 years after soil translocation

was observed by Budge et al. (2011). The increased

Q10 values with warming might also be linked to the

greater amount of respired biochemically recalcitrant

SOM, which has greater temperature sensitivity

(Craine et al. 2010). It was very likely that labile C

would drastically decline at the end of the warming

experiment, forcing microbes to rely on more

recalcitrant soil C.

In contrast, Q10 and R10 were not affected by

transferring soil monoliths from the low to the high-

elevation site (Table 2), suggesting that the tempera-

ture reduction might be within the range of tolerance

limits for normal microbial activity, or the phenom-

enon represented a chronic response (or acclimation,

adaptation) of microbial community to cooling. The

fact that soils from the high and low-elevation sites

differ in their properties, for example soil C and N

content, could also cause the different warming and

cooling effects observed. However, we did not find

significant effect of soil origin on both Q10 and qCO2

(Table 3). Therefore, Q10 was mainly affected by

transfer of the soils. Although different methods used

to calculate Q10 might lead to different results

(Zimmermann et al. 2009), Q10 calculated by use of

both the van’t Hoff (the most commonly used

equation) and the Lloyd and Taylor (suggested to

give an unbiased estimate of Q10) equations had

consistent responses to the treatments in our study.

The Q10 calculation can be affected by the range of

temperature considered (Katterer et al. 1998; Paz-

Ferreiro et al. 2012). However, the positive warming

effect on Q10 in our study was apparently not caused

by the different temperature range, because lower

temperature sensitivity were estimated at higher

temperatures (Katterer et al. 1998). The positive

warming effects on Q10 values must be further

studied, because this translocation experiment was

conducted for one year only. It is reported that a

sustained temperature increase may reduce the

a bFig. 5 Relationships

between qCO2 and Q10

values calculated on the

basis of both the van’t Hoff

and Lloyd and Taylor

equations


123

temperature sensitivity of soil OM decomposition

(Craine et al. 2013). Therefore, the response of soil

OM decomposition to warming might be a nonlinear

process, along with depletion of soil labile carbon

(Bradford et al. 2008) and the adaptation of microbes

to the new environment (Bradford et al. 2008;

Crowther and Bradford 2013; Luo et al. 2001). The

acclimation or adaptation of microbes to warming has

been widely reported (Luo et al. 2001; Bradford et al.

2008), and it is important to understand microbial

response to cooling, with implications for modeling of

paleoclimate (e.g., Holocene), particularly during

periods of regional or global cooling. Further research

is needed to broaden our understanding of possible

mechanisms causing different responses to cooling

and warming.

Conclusions

The simulated warming treatment (transfer of soils

from the high to the low-elevation site) altered soil

OM decomposition processes, including increased soil

surface CO2 flux and labile organic C (i.e., K2SO4-C)

production. Therefore, a large amount of soil C loss

occurred in the early stage of warming and such C

losses were linked to the increased extractable organic

C (K2SO4-C) supply under warming. The simulated

cooling reduced CO2 flux, but the extent of decrease in

C loss (30 %) was lower than the extent of increase in

C loss (44 %) caused by simulated warming. Further-

more, cooling did not cause the expected opposite

changes in labile organic C and decomposition

behavior. We therefore conclude that cooling and

warming had different effects on soil organic C

processes. Such different effects should be taken into

consideration in paleoecological modeling when both

warming and cooling are involved in changes in the

regional and global climate.

Acknowledgments We gratefully acknowledge the support of

Yin Wu, Ye Tian, Xinfang Yang, Xiaojing Liu, Song Yao, and

Jiguo Liu of the Baotianman National Nature Reserve for their

assistance in field monitoring and sampling. We are grateful to

professor Pu Mu of Beijing Normal University and the three

anonymous reviewers for their valuable comments on an earlier

version of the manuscript. This study was jointly funded by

China’s National Natural Science Foundation (No. 31290223),

the Ministry of Finance (No. 201104006, 201404201), the

Ministry of Science and Technology (2012BAD22B01), and

CFERN and GENE Award Funds on Ecological Paper.

Open Access This article is distributed under the terms of the

Creative Commons Attribution License which permits any use,

distribution, and reproduction in any medium, provided the

original author(s) and the source are credited.

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